Accumulation of transposable elements in selfing populations of Arabidopsis lyrata supports the ectopic recombination model of transposon evolution

Abstract

Transposable elements (TE) can constitute a large fraction of plant genomes, yet our understanding of their evolution and fitness effect is still limited. Here we tested several models of evolution that make specific predictions about differences in TE abundance between selfing and outcrossing taxa, and between small and large populations. We estimated TE abundance in multiple populations of North American Arabidopsis lyrata differing in mating system and long-term size, using transposon insertion display on several TE families. Selfing populations had higher TE copy numbers per individual and higher TE allele frequencies, supporting models which assume that selection against TEs acts predominantly against heterozygotes via the process of ectopic recombination. In outcrossing populations differing in long-term size, the data supported neither a model of density-regulated transposition nor a model of direct deleterious effect. Instead, the population structure of TEs revealed that outcrossing populations tended to split into western and eastern groups - as previously detected using microsatellite markers - whereas selfing populations from west and east were less differentiated. This, too, agrees with the model of ectopic recombination. Overall, our results suggest that TE elements are nearly neutral except for their deleterious potential to disturb meiosis in the heterozygous state.

Snake W Sex Chromosome: The Shadow of Ancestral Amniote Super-Sex Chromosome

“…Weaker selection against the insertion of additional TEs leads to their accumulation under a lack of recombination. Moreover, TEs can promote ectopic recombination, facilitating genomic rearrangement to further suppress recombination [162]. The heterochromatic regions in amniotes are also predominantly accumulated by satellite DNA, in a class of repeats characterized by a tandem arrangement with highly repeated monomeric units longer than 100 bp, or simple repeats, such as mini-(>10 and <100 bp) and microsatellites (usually <10 bp) [163,164].…”

Bursts of transposable elements and adaptive evolution of fig wasps

“…All these characters provide a greater possibility for non-pollinators to increase the types of TEs, especially the number and total length. Inbreeding reproduction will influence the mutation accumulation in genomes by affecting the N e (Lefebure, Morvan et al 2017, Bonchev andWilli 2018), as small N e will exacerbate accumulation of deleterious mutations including TEs (Willemsen, Cui et al 2020). Within 1 Ma, the N e of pollinating fig wasps was smaller and in a state of fluctuating contraction, which was consistent with the situation that many genes in this group were subjected to positive selection.…”

Causes and consequences of linkage disequilibrium among transposable elements within eukaryotic genomes

“…While transcriptional and post-transcriptional silencing of TEs correspond to plausible mechanisms generating copy-number-dependent transposition (Deniz et al, 2019; Kelleher et al, 2020; Almeida et al, 2022), ectopic recombination has been identified as a possible source of synergistic epistasis among elements (Montgomery et al, 1987; Langley et al, 1988). Indirect evidence suggests that ectopic recombination likely plays an important role in the containment of TEs (Bartolomé et al, 2002; Song and Boissinot, 2007; Petrov et al, 2011; Bonchev and Willi, 2018); however, to what extent this process generates synergistic selection against TE copies remains difficult to test. Recently, Lee (2022) used population genomic data from D. melanogaster to infer the degree of synergism among TEs from patterns of linkage disequilibrium between elements, based on the assumption that synergistic epistasis generates negative LD.…”

“…However, it is possible that extant asexual species originated from sexual ancestors in which the level of TE activity was low, while new asexual lineages in which TE activity is high tend to go extinct due to TE accumulation (Arkhipova and Meselson, 2005a), and it would thus be of interest to explore TE dynamics in newly derived asexual lineages. Transitions towards self-fertilization may also either lead to an increased or decreased efficiency of selection against TEs depending on the relative importance of deterministic and stochastic forces, with the additional effect that homozygosity may decrease the rate of ectopic recombination among elements (Montgomery et al, 1991; Wright and Schoen, 1999; Morgan, 2001; Bonchev and Willi, 2018). Measuring LD among TEs in selfing or asexual populations (and contrasting LD within and between TE families) may shed further light on the selective forces acting on TEs, and should be made easier by the recent development of long-reads sequencing technologies.…”